Mammalian development in space.

Life on Earth, and thus the reproductive and ontogenetic processes of all extant species and their ancestors, evolved under the constant influence of the Earth's l g gravitational field. These considerations raise important questions about the ability of mammals to reproduce and develop in space. In this chapter, I review the current state of our knowledge of spaceflight effects on developing mammals. Recent studies are revealing the first insights into how the space environment affects critical phases of mammalian reproduction and development, viz., those events surrounding fertilization, embryogenesis, pregnancy, birth, postnatal maturation and parental care. This review emphasizes fetal and early postnatal life, the developmental epochs for which the greatest amounts of mammalian spaceflight data have been amassed. The maternal-offspring system, the coordinated aggregate of mother and young comprising mammalian development, is of primary importance during these early, formative developmental phases. The existing research supports the view that biologically meaningful interactions between mothers and offspring are changed in the weightlessness of space. These changes may, in turn, cloud interpretations of spaceflight effects on developing offspring. Whereas studies of mid-pregnant rats in space have been extraordinarily successful, studies of young rat litters launched at 9 days of postnatal age or earlier, have been encumbered with problems related to the design of in-flight caging and compromised maternal-offspring interactions. Possibilities for mammalian birth in space, an event that has not yet transpired, are considered. In the aggregate, the results indicate a strong need for new studies of mammalian reproduction and development in space. Habitat development and systematic ground-based testing are important prerequisites to future research with young postnatal rodents in space. Together, the findings support the view that the environment within which young mammals develop, comprised of its mother and siblings, is of paramount importance in interpreting spaceflight effects.

[1]  S. Reppert,et al.  Direct in utero perception of light by the mammalian fetus. , 1989, Brain research. Developmental brain research.

[2]  C. Gharib,et al.  Cardiac atrial natriuretic peptide (ANP) in rat dams and fetuses developed in space (NIH-R1 and NIH-R2 experiments). , 1999, Life sciences.

[3]  M. Hofer,et al.  Baroreceptor sensitivity in two-week-old rat pups: effects of nutrient deprivation and sino-aortic denervation , 1988, Physiology & Behavior.

[4]  I. Fish,et al.  Effect of malnutrition on regional growth of the developing rat brain. , 1969, Experimental neurology.

[5]  M. Hofer The Mother-Infant Interaction as a Regulator of Infant Physiology and Behavior , 1983 .

[6]  R. Bridges Endocrine regulation of parental behavior in rodents. , 1990 .

[7]  R. Llinás,et al.  Spaceflight induces changes in the synaptic circuitry of the postnatal developing neocortex. , 2002, Cerebral cortex.

[8]  L V Serova,et al.  Early postnatal development of rats gestated during flight of Cosmos 1514. , 1985, The Physiologist.

[9]  R. Kalb,et al.  Experience-Dependent Development of Spinal Motor Neurons , 2000, Neuron.

[10]  M. Meaney,et al.  Naturally Occurring Differences in Maternal Care are Associated with the Expression of Oxytocin and Vasopressin (V1a) Receptors: Gender Differences , 2002, Journal of neuroendocrinology.

[11]  D. Hubel,et al.  Early Exploration of the Visual Cortex , 1998, Neuron.

[12]  P. K. Anokhin,et al.  Systemogenesis as a General Regulator of Brain Development , 1964 .

[13]  K. Godfrey,et al.  Fetal programming and adult health , 2001, Public Health Nutrition.

[14]  J. Alberts,et al.  Perinatal stimulation and adaptation of the neonate , 1996, Acta paediatrica (Oslo, Norway : 1992). Supplement.

[15]  A. M. Wong,et al.  Rat gestation during space flight: Outcomes for dams and their offspring born after return to earth , 1997, Integrative physiological and behavioral science : the official journal of the Pavlovian Society.

[16]  J. Altman,et al.  The influence of nutrition on neural and behavioral development. IV. Effects of infantile undernutrition on the growth of the cerebellum. , 1972, Developmental psychobiology.

[17]  F. Champagne,et al.  Maternal Care, Gene Expression, and the Development of Individual Differences in Stress Reactivity , 1999, Annals of the New York Academy of Sciences.

[18]  T. Shimizu Development of the aortic baroreflex system under conditions of microgravity. , 1999, Journal of gravitational physiology : a journal of the International Society for Gravitational Physiology.

[19]  K Walton,et al.  Changes in gravity influence rat postnatal motor system development: from simulation to space flight. , 1997, Gravitational and space biology bulletin : publication of the American Society for Gravitational and Space Biology.

[20]  J. Oyama,et al.  Growth and development of mice and rats conceived and reared at different G-intensities during chronic centrifugation. , 1985, The Physiologist.

[21]  W. P. Smotherman Mother-infant interaction and the modulation of pituitary-adrenal activity in rat pups after early stimulation. , 1983, Developmental psychobiology.

[22]  C. Gharib,et al.  Choroidal responses in microgravity. (SLS-1, SLS-2 and hindlimb-suspension experiments). , 1995, Acta astronautica.

[23]  R E Grindeland,et al.  Comparison of hyper- and microgravity on rat muscle, organ weights and selected plasma constituents. , 1998, Aviation, space, and environmental medicine.

[24]  A. Ronca,et al.  Models to Study Gravitational Biology of Mammalian Reproduction1 , 2002, Biology of reproduction.

[25]  L. Bruce,et al.  The development of vestibular connections in rat embryos in microgravity. , 1997, Journal of gravitational physiology : a journal of the International Society for Gravitational Physiology.

[26]  C. Escobar,et al.  Dendritic branching of claustral neurons in neonatally undernourished rats. , 1995, Biology of the neonate.

[27]  L. Rosenblum,et al.  Symbiosis in Parent-Offspring Interactions , 1983 .

[28]  J. Alberts,et al.  Effects of space flight on the immunohistochemical demonstration of connexin 26 and connexin 43 in the postpartum uterus of rats. , 1999, Journal of reproduction and fertility.

[29]  Kerry Walton,et al.  Postnatal development under conditions of simulated weightlessness and space flight , 1998, Brain Research Reviews.

[30]  Bonnie P. Dalton,et al.  Neurolab: Final Report for the Ames Research Center Payload , 2002 .

[31]  J R Alberts,et al.  Effects of prenatal spaceflight on vestibular responses in neonatal rats. , 2000, Journal of applied physiology.

[32]  J. Jeffrey,et al.  Collagenase and Tissue Plasminogen Activator Production in Developing Rat Calvariae: Normal Progression Despite Fetal Exposure to Microgravity , 1998, Calcified Tissue International.

[33]  R B Johnson,et al.  The bearable lightness of being: Bones, muscles, and spaceflight , 1998, The Anatomical record.

[34]  J. Altman,et al.  The influence of nutrition on neural and behavioral development. 3. Development of some motor, particularly locomotor patterns during infancy. , 1971, Developmental psychobiology.

[35]  G Sonnenfeld,et al.  Spaceflight and development of immune responses. , 1998, Journal of applied physiology.

[36]  S. Langley-Evans Fetal programming of cardiovascular function through exposure to maternal undernutrition , 2001, Proceedings of the Nutrition Society.

[37]  A. Silverstein From the forehead of Zeus: The ontogeny of the immune response , 1995, Eye.

[38]  Emily R Morey-Holton,et al.  Hindlimb unloading rodent model: technical aspects. , 2002, Journal of applied physiology.

[39]  W. Oosterveld,et al.  Altered Behaviour in Hamsters Conceived and Born in Hypergravity , 1997, Brain Research Bulletin.

[40]  A. Ronca,et al.  Sampling of prenatal and postnatal offspring from individual rat dams enhances animal use without compromising development. , 1996, Contemporary topics in laboratory animal science.

[41]  D J Wolgemuth,et al.  Models and molecular approaches to assessing the effects of the microgravity environment on vertebrate development. , 1995, ASGSB bulletin : publication of the American Society for Gravitational and Space Biology.

[42]  Wassersug,et al.  Swimming kinematics and respiratory behaviour of xenopus laevis larvae raised in altered gravity , 1998, The Journal of experimental biology.

[43]  F. Gaven,et al.  Development of the rat efferent vestibular system on the ground and in microgravity. , 2001, Brain research. Developmental brain research.

[44]  Rupert Gerzer Space physiology and medicine , 1982 .

[45]  V R Edgerton,et al.  Neuromuscular adaptation to actual and simulated weightlessness. , 1994, Advances in space biology and medicine.

[46]  K. Ijiri Fish mating experiment in space--what it aimed at and how it was prepared. , 1995, Uchu Seibutsu Kagaku.

[47]  M. Ghandour,et al.  Effects of an 11-day spaceflight on the choroid plexus of developing rats. , 1997, Brain research. Developmental brain research.

[48]  J. Day,et al.  Maternal care, hippocampal synaptogenesis and cognitive development in rats , 2000, Nature Neuroscience.

[49]  C. Hodson,et al.  Effects of space flight on ovarian-hypophyseal function in postpartum rats. , 1997, Journal of Reproduction and Fertility.

[50]  N. Krasnegor,et al.  Mammalian parenting : biochemical, neurobiological, and behavioral determinants , 1990 .

[51]  C. L. Moore The Role of Maternal Stimulation in the Development of Sexual Behavior and Its Neural Basis a , 1992, Annals of the New York Academy of Sciences.

[52]  G. Adams,et al.  Effects of spaceflight and thyroid deficiency on hindlimb development. I. Muscle mass and IGF-I expression. , 2000, Journal of applied physiology.

[53]  S. Levine Primary social relationships influence the development of the hypothalamic–pituitary–adrenal axis in the rat , 2001, Physiology & Behavior.

[54]  J. Oyama,et al.  Reproduction and growth of mice and rats under conditions of simulated increased gravity. , 1967, The American journal of physiology.

[55]  N D Stull,et al.  Induction of a dopaminergic phenotype in cultured striatal neurons by bone morphogenetic proteins. , 2001, Brain research. Developmental brain research.

[56]  H. Lagercrantz,et al.  The "stress" of being born. , 1986, Scientific American.

[57]  A. Ronca,et al.  Physiology of a microgravity environment selected contribution: effects of spaceflight during pregnancy on labor and birth at 1 G. , 2000, Journal of applied physiology.

[58]  J. Miquel,et al.  Gravity effects on reproduction, development, and aging. , 1991, Advances in space biology and medicine.

[59]  Elizabeth A Thom,et al.  Frequency of uterine contractions and the risk of spontaneous preterm delivery. , 2002, The New England journal of medicine.

[60]  S. Schanberg,et al.  Responses to maternal separation : mechanisms and mediators , 1998, International Journal of Developmental Neuroscience.

[61]  K. Walton,et al.  Space flight affects magnocellular supraoptic neurons of young prepuberal rats: transient and permanent effects. , 2001, Brain research. Developmental brain research.

[62]  J R Alberts,et al.  Effects of gravity on development: the importance of behavior. , 1999, Journal of gravitational physiology : a journal of the International Society for Gravitational Physiology.

[63]  D A Riley,et al.  Effects of hindlimb unloading on neuromuscular development of neonatal rats. , 2000, Brain research. Developmental brain research.

[64]  T. Casey,et al.  The effects of spaceflight on mammary metabolism in pregnant rats. , 1999, Proceedings of the Society for Experimental Biology and Medicine. Society for Experimental Biology and Medicine.

[65]  O. Gazenko Ontogenesis of mammals in microgravity , 1993 .

[66]  F. Haddad,et al.  Effects of spaceflight and thyroid deficiency on rat hindlimb development. II. Expression of MHC isoforms. , 2000, Journal of applied physiology.

[67]  C. Wade,et al.  Maternal Reproductive Experience Enhances Early Postnatal Outcome Following Gestation and Birth of Rats in Hypergravity1 , 2001, Biology of reproduction.

[68]  Spatial Learning and Memory Is Preserved in Rats after Early Development in a Microgravity Environment , 2002, Neurobiology of Learning and Memory.

[69]  C S Leach,et al.  The endocrine system in space flight. , 1988, Acta astronautica.

[70]  M. Fejtek,et al.  Effects of laparotomy, cage type, gestation period and spaceflight on abdominal muscles of pregnant rodents. , 1999, The Journal of experimental zoology.

[71]  M. Inobe,et al.  Effects of microgravity on myogenic factor expressions during postnatal development of rat skeletal muscle. , 2002, Journal of applied physiology.

[72]  A. R. Elliott,et al.  Sleep, performance, circadian rhythms, and light-dark cycles during two space shuttle flights. , 2001, American journal of physiology. Regulatory, integrative and comparative physiology.